Báo cáo sinh học: " Macrogeographic patterns in B-chromosome and inversion polymorphisms of the grasshopper" pps

Original
article
Macrogeographic
patterns
in
B-chromosome
and
inversion
polymorphisms
of
the
grasshopper
Trimerotropis
pallidipennis
VA
Confalonieri
Universidad
de
Buenos
Aires,
Facultad
de
Ciencias
Exactas
y
Naturales,
Departamento
de
Ciencias
BioLÓgicas,
Intendente

Güiraldez
y Costanera
Norte,
(1428)
Buenos
Aires,
Argentina
(Received
10
June
1994;
accepted
16
February
1995)
Summary -
South
American
populations
of
Trimerotropis
pallidipennis
are
polymorphic
for
pericentric
inversions
and
B-chromosomes.
Previous

studies
revealed
the
existence
of
altitudinal,
latitudinal
and
longitudinal
clines
for
9
chromosomal
sequences,
whose
repetition
in
independent
groups
of
populations
and
over
a
wide
area
suggested
the
action
of

natural
selection.
The
frequencies
of
B-chromosomes
were
analyzed
in
25
samples
from
Argentina.
In
some
of
them,
the
B-chromosome
interfers
with
the
genetic
control
of
chiasma
formation,
which
is
partly

conditioned
by
inversions.
Multiple
regression
analyses
revealed
that
the
frequency
of
B-carriers
in
each
population
is
significantly
associated
with
latitude
(negatively)
and
longitude
(positively),
and
that
the
frequency
of
inversions

significantly
decreases
at
higher
altitudes
and
latitudes.
The
pattern
of
distribution
observed
for
B-carriers
is
most
probably
related
to
the
suitability
of habitats.
These
results
agree
with
the
parasitic
model,
which

claims
that
higher
incidence
of
the
B-chromosome
in
natural
populations
is
associated
with
more
favorable
environments.
Orthoptera
/
polymorphism
/
B-chromosome
/
natural
selection
/
inversion
Résumé -
Répartition
macrogéographique
des

polymorphismes
du
chromosome
B
et
d’inversion
chez
la
sauterelle
T
rhnerotropjs
pallidipennis.
Les
populations
sud-
américaines
de
Trimerotropis
pallidipennis
sont
polymorphes
pour
des
inversions
péri-
centriques
et
les
chromosomes
B.

Les
études
antérieures
ont
révélé
l’existence
de
clines
altitudinaux,
latitudinaux
et
longitudinaux
pour
neuf
séquences
chromosomiques,
dont
les
répétitions
dans
des
groupes
indépendants
de
populations
et
sur
une
vaste
région

suggèrent
l’action
de la
sélection
naturelle.
Les
fréquences
des
chromosomes
B
ont
été
analysées
dans
!5
populations
d’Argentine.
On
peut
observer
que
dans
quelques
échantillons
le
chromosome
B
intervient
dans
le

contrôle
génétique
de
la
formation
du
chiasma,
qui
est
conditionné
partiellement
par
les
inversions.
Une
analyse
de
régression
multiple
révèle
que
la
fréquence
des
porteurs
de
B
dans
chaque
population

est
associée
significativement
à
leur
situation
en
latitude
(négativement)
et
longitude
(positivement),
et
que la
fréquence
des
inversions
diminue
significativement
en fonction
de
l’altitude
et
de
la
latitude.
Le
modèle
de
distribution

observé
pour
les
porteurs
de
B
est
très
probablement
en
relation
avec
la
qualité
des
habitats.
Les
résultats
concordent
avec
le
modèle
parasitaire
selon
lequel
de
hautes
fréquences
du
chromosome

B
dans
les
populations
naturelles
sont
associées
à
des
conditions
plus
favorables
de
milieu.
orthoptère
/
polymorphisme
/
chromosome
B
/
inversion
/
sélection
naturelle
INTRODUCTION
South
American
populations
of

Trimerotropis
pallidipennis
(Orthoptera)
(2n
=
23
d
XO)
are
particularly
interesting
from
an
evolutionary
standpoint
because
of
the
occurrence
of
pericentric
inversions
and
B-chromosome
polymorphisms
(Mesa,
1971;
Vaio
et
al,

1979;
Gobi
et
al,
1985;
Confalonieri,
1988,
1994;
Confalonieri
and
Colombo,
1989)
contrasting
with
North
American
populations
that
are
structurally
monomorphic
(Coleman,
1948;
White,
1949,
1951).
Previous
studies
revealed
the

existence
of
altitudinal,
latitudinal
and
longitudinal
clines
for
9
chromosomal
sequences,
whose
repetition
in
independent
groups
of
populations
and
over
a
wide
area
suggested
that
natural
selection
maintains
these
polymorphisms

(Confalonieri
and
Colombo,
1989;
Confalonieri,
1994).
Minimum
temperature
and
humidity
were
considered
as
the
possible
selective
agents.
With
respect
to
genetic
recombination,
inversion
polymorphisms
are
also
associated
to
an
important

chiasma
localization
(usually
near
or
at
telomeric
positions),
which
leads
to
an
inverse
association
between
total
chiasma
frequency
and
the
mean
number
of
heteromorphic
bivalents
per
male
(H)
(Goni
et

al,
1985;
Confalonieri,
1988).
A
B-chromosome
was
observed
in
almost
every
population
from
Argentina
and
in
some
of
them
this
chromosome
is
presumably
interfering
with
the
genetic
control
of
chiasma

conditions
(Confalonieri,
1992).
The
present
paper
reports
a
macrogeographic
pattern
of
distribution
of
B-frequencies
in
relation
to
those
of
inversion
sequences.
These
results
are
dis-
cussed
in
the
light
of

the
parasitic
and
heterotic
models
of
maintenance
of
B
poly-
morphisms.
MATERIALS
AND
METHODS
Twenty-five
samples
of
T
pallidipennis
collected
in
several
provinces
of
Argentina
were
cytologically
analyzed
(table
I);

159
males
belonging
to
some
of
these
samples
were
previously
studied
for
chiasma
conditions
(Confalonieri,
1992).
Testes
were
fixed
in
1:3
acetic
acid/ethanol
and
squashed
in
acetic
orcein.
In
order

to
weight
the
regression
analysis,
B-chromosome
frequences
were
trans-
formed
according
to
the
method
of
Christiansen
et
al
(1976),
which
takes
into
account
differences
in
sample
size.
In
Uspallata,
data

correspond
to
the
sample
of
1991.
N:
sample
size.
B:
B-chromosome
carrier
frequency.
H:
mean
number
of heteromorphic
bivalents
per
male.
I:
mean
number
of
inverted
chromosomes
per
male.
ALT:
altitude

in
meters.
LAT
and
LONG:
south
latitude
and
west
longitude
in
degrees.
*
Data
from
Confalonieri
and
Colombo
(1989).
**
Data
from
Goni
et
al
(1985).
RESULTS
Karyotype,
B-chromosome
and

inversion
systems
The
basic
male
karyotype
of
T
pallidipennis
consists
of
2n
=
23
chromosomes
which
can
be
grouped
into
3
size
classes:
large
(L1-L3);
medium
(M4-M8),
including
the
X-chromosome;

and
short
(S9-S11).
The
X-chromosome
is
metacentric,
the
large
elements
are
submetacentric
(Vaio
et
al,
1979)
while
both
medium
and
short
chromosomes
are
basically
acrocentric
(Confalonieri,
1988).
The
B-chromosome
has

a
distal
heterochromatic
X-like
segment
and
a
proximal
isopycnotic
region,
and
is
a
little
larger
in
size
than
the
S9
chromosome
(Mesa,
1971;
Vaio
et
al,
1979;
Gofii
et
al,

1985;
Confalonieri,
1988).
In
C-banded
cells,
it
shows
2
interstitial
positively
stained
bands which
coincide
with
part
of
the
heterochromatic
region
(Sanchez
and
Confalonieri,
1993).
Furthermore,
it
is
mitotically
and
meiotically

stable.
The
frequencies
of
carriers
in
each
sample
are
indicated
in
table
I.
In
Uspallata,
stability
of
B-frequency
was
demonstrated
in 2
consecutive
samples
collected
in
1991
and
1992
and
with

respect
to
a
sample
of
1984.
Six
pericentric
inversions
involve
4
of
the
medium-sized
chromosomes,
producing
multiple
karyomorphs
in
polymorphic
populations
(Vaio
et
al,
1979;
Goni
et
al,
1985;
Confalonieri

and
Colombo,
1989).
Macrogeographic
patterns
In
order
to
assess
possible
patterns
of
distribution
of
B-frequencies,
data
from
20
samples
collected
in
a
wide
altitudinal
(ALT),
latitudinal
(LAT)
and
longitudinal
(LONG)

range
were
used
in
addition
to
5
samples
from
south
Argentina
reported
in
Goni
et
al
(1985).
Table
I
shows
the
frequencies
of B-carriers
in
each
sample,
together
with
the
mean

number
of
heteromorphic
bivalents
(H)
and
inversions
(I)
per
male
per
population.
Results
of
multiple
regression
of
these
3
dependent
variables
on
ALT,
LONG
and
LAT
are
presented
in
table

II.
Two
distinct
patterns
of
variation
were
observed
for
2
kinds
of
polymorphisms.
The
first
clear
pattern
is
demonstrated
for
supernumerary
chromosomes
so
that
the
frequency
of
B-carriers
in
each

sample
is
significantly
associated
with
its
latitudinal
and
longitudinal
situation.
Secondly,
the
frequency
of
inversions
is
highly
associated
with
latitude
and
altitude
in
such
a
way
that inversions
tend
to
disappear

at
higher
latitudes
and
altitudes.
As
previously
shown
(Confalonieri
and
Colombo,
1992),
both
clines
indeed
reflect
a
minimum
temperature
dependence.
The
level
of
inversion
polymorphism
(measured
through
the
parameter
H)

did
not
show
a
clear
macrogeographic
pattern
of
variation
because
maximal
values
are
attained
at
intermediate
altitudes
and
latitudes,
so
the
clines
observed
depend
on
which
groups
of
populations
are

scored.
T
pallidipennis,
which
is
endemic
to
North
America,
is
1
of
the
few
trimero-
tropines
to
have
successfully
extended
its
distribution
to
Andean
South
America
(Vaio
et
al,
1979),

being
adapted
here
to
a
wide
altitudinal
range.
Rain
forests
and
humid_grasslands
(in
eastern
localities)
are
not
inhabited
by
this
species
and
its
basic
requirement
appears
to
be
the
prevalence

of
arid
and
semi-arid
conditions.
This
species
is
not
present
at
southern
latitudes.
In
fact,
data
from
Goni
et
al
(1985)
(table
I)
correspond
to
populations
considered
by
these
authors

as
marginal,
because
they
are
situated
at
the
southern
border
of
the
species
range.
Therefore,
more
eastern
longitudes
and
southern
latitudes
are
most
probably
marginal
environments
for
T
pallidipennis,
just

where
the
frequency
of
B-carriers
tends
to
be
lower.
DISCUSSION
The
longstanding
debate
about
B-chromosomes
revolves
around
the
issue
of
whether
these
widespread
polymorphisms
are
simply
a
direct
result
of

the
accu-
mulation
mechanisms
or
whether
they
derive
from
the
action
of
natural
selection
(Jones,
1985).
The
view
presently
favored
inclines
to
the
so-called
’parasitic’
model
which
argues
that
B-chromosomes

are
selfish
elements
and
drive
is
the
main
force
generating
this
kind
of
polymorphism
(Jones,
1991;
Shaw
and
Hewitt,
1991).
An
extreme
case
of
selfishness
has
been
recently
reported
by

Nur
et
al
(1988).
However,
a
great
variety
of
mechanisms
of
drive,
phenotypic
effects
and
origins
have
been
described
for
B-carriers
belonging
to
different
species
and
even
to
populations
of

the
same
species
(Jones
and
Rees,
1982;
Jones,
1985,
1991;
Bell
and
Burt,
1990;
Shaw
and
Hewitt,
1991;
Bougourd,
1993).
It
thus
seems
inappropriate
to
unequivocally
ascribe
a
universal
model

of
maintenance
for
all
B-chromosome
polymorphisms.
The
2
distinct
patterns
of
variation
observed
for
both
B-chromosomes
and
structural
rearrangements
in
T
pallidipennis
correspond
to
different
processes
of
evolution.
All
inverted

sequences
tend
to
increase
in
frequency
towards
lower
altitudes
and
latitudes.
These
clines
probably
respond
to
geographically
varying
selection
related
to
some
climatic
variables
(Confalonieri,
1994).
Moreover,
some
enzymatic
loci

could
be
in
linkage
disequilibrium
with
supergenes
maintained
by
inversions,
which
might
be
the
target
of
selection.
The
clines
observed
for
supernumerary
chromosomes
following
geographical
variables
are
better
explained
by

means
of
the
parasitic
model:
B-carriers
are
obviously
most
frequent
in
those
areas
where
the
species
thrive
and
disappear
in
circumstances
where
the
burden
on
fitness
is
too
heavy
to

bear,
ie
in
marginal
environments.
Similar
situations
were
found
in
Mymneleotettiz
maculatus,
where
B-carriers
are
limited
to
populations
in
the
south
and
east
of
Great
Britain
which
are
climatically
better

for
grasshoppers
(Hewit
and
Brown,
1970;
Hewitt,
1973),
and
in
Crepis
capillaris,
where
higher
B-frequencies
are
also
the
reflection
of
the
suitability
of
the
habitats
(Parker
et
al,
1991).
Some

of
the
phenotypic
effects
of
B-chromosomes
concerned
with
recombination
at
meiosis
have
often
been
considered
to
be
of
adaptive
importance
(Jones
and
Rees,
1982).
However,
this
view
has
recently
been

reconsidered
(Bell
and
Burt,
1990;
Shaw
and
Hewitt,
1991).
Bell
and
Burt
(1990)
proposed
the
theory
of
’inducible
recombination’
by
which
individuals
with
’parasitic’
B-carriers
might
be
expected
to
increase

recombination
amongst
the
autosomes
so
that
new
genetic
variants
that
are
resistant
to
infection
by
B-carriers
would
be
more
likely
to
arise.
In
fact,
the
presence
of
B-carriers
is
usually

associated
with
an
increase
in
chiasma
formation
(Jones
and
Rees,
1985;
Bell
and
Burt,
1990).
On
this
theory,
successful
’B-parasites’
would
be
expected
to
reduce
the
rate
of
recombination
of

their
hosts.
In
T
pallidipennis
a
significant
decrease
of
mean
chiasma
frequency
of
B-carriers
was
verified
for
some
populations
(Confalonieri,
1992).
This
effect
of
B-chromosomes
could
then
be
of
significance

to
the
long-term
survival
and
evolution
of
local
populations,
especially
those
in
less
favorable
environments.
ACKNOWLEDGMENTS
I
wish
to
express
my
sincere
thanks
to
JH
Hunziker
for
critical
reading
of

the
manuscript.
Financial
support
from
the
Consejo
Nacional
de
Investigaciones
Cientificas
y
T6cnicas
and
Universidad
de
Buenos
Aires,
through
grants
to
JH
Hunziker
and
JC
Vilardi.
REFERENCES
Bell
G,
Burt

A
(1990)
B-chromosomes:
germ-line
parasites
which
induce
changes
in
host
recombination.
Parasitology
100,
S19-S26
Bougourd
S
M
(1993)
Phenotypic
effects.
In:
Abstracts
of
the
lst
B-chromosome
Confer-
ence.
Madrid,
21-25

September
1993
(Universidad
Aut6noma
de
Madrid,
ed),
58-62
Christiansen
FB,
Frydenberg
0,
Hjorth
JP,
Simonsen
V
(1976)
Genetics
of
Zoarces
populations
IX.
Geographic
variation
at
three
phosphoglucomutase
loci.
Hereditas
83,

245-286
Coleman
LC
(1948)
The
cytology
of
some
western
species
of
Trimerotropis
(Acrididae).
Genetics
33,
519-528
Confalonieri
VA
(1988)
Effects
of
centric-shift
polymorphisms
on
chiasma
conditions
in
Trimerotropis
pallidipennis
(Oedipodinae:

Acrididae).
Genetica
76,
171-179
Confalonieri
VA
(1992)
B-chromosomes
of
Trimerotro
P
is
P
allidipennis:
new
effects
on
chiasma
conditions.
Caryologia
45,
145-153
Confalonieri
VA
(1994)
Inversion
polymorphisms
and
natural
selection

iW
’rimerotro
P
is
pallidipennis
(Orthoptera):
correlations
with
geographical
variables.
Hereditas
121,
78-
86
Confalonieri
VA,
Colombo
PC
(1989)
Inversion
polymorphisms
in
TW
merotropM
pal-
lidipennis
(Orthoptera):
clinal
variation
along

an
altitudinal
gradient. Heredity 62,
107-
112
Confalonieri
VA,
Colombo
PC
(1992)
Polimorfismos
de
inversion
y
selecci6n
natural
en
Trimerotro!is
pallidipennis:
correlaci6n
con
variables
climaticas.
Actas
XXIII
Congreso
Argentino
de
Gen6tica,
Pergamino,

Argentina
(Sociedad
Argentina
de
Genetica,
ed),
20
Goni
B,
de
Vaio
E,
Beltrami
M
et
al
(1985)
Geographic
patterns
of
chromosomal
variation
in
populations
of
the
grasshopper
(Trimerotropis
pallidipennis)
from

southern
Argentina.
Can
J
Genet
Cytol
27,
259-271
Hewitt
G
M
(1973)
Evolution
and
maintenance
of
B-chromosomes.
Chromosomes
Today
4,
351-369
Hewitt
G
M,
Brown
F
M
(1970)
The
B-chromosome

system
of
Myrmeleotettix
mac!latus.
V.
A
steep
cline
in
East
Anglia.
Heredity
25,
363-371
Jones
RN,
Rees
H
(1982)
B-chromosomes.
Academic
Press,
New
York,
USA
Jones
RN
(1985)
Are
B

chromosomes
‘selfish’?
In:
The
Evolution
of
Genome
Size
(T
Cavalier-Smith,
ed),
John
Wiley
&
Sons,
London,
UK,
397-425
Jones
RN
(1991)
B-chromosomes
drive. Am
Nat
137,
430-442
Mesa
A
(1971)
Polimorfismo

cromos6mico
en
Trimerotropis
pallidipennis
(Orthoptera-
Acridoidae-Oedipodinae).
Rev
Per
Entom
14,
2
Nur
U,
Werren
J,
Eickbush
D,
Burke
D,
Eickbush
T
(1988)
A
’selfish’
B
chromosome
that
enhances
its
transmission

by
eliminating
the
paternal
genome.
Science
240,
512-514
Parker
J
S,
Jones
G
H,
Edgar
L
A,
Whitehouse
C
(1991)
The
population
cytogenetics
of
Crepis
capillaris
IV.
The
distribution
of

B-chromosomes
in
British
populations.
Heredity
66, 211-218
Sanchez
V,
Confalonieri
V
(1993)
Chromosome
banding
pattern
in
1’rimerotropis
pal-
lidipennis
(Orthoptera:
Acrididae).
Cytobios
73,
105-110
Shaw
D,
Hewitt
G
(1991)
B-chromosomes,
selfish

DNA
and
theoretical
models:
where
next?
In:
Oxford
Surveys
in
Evolutionary
Biology
(D
Futuyma,
J
Antonovics,
eds),
Oxford
University
Press,
Oxford,
OK,
Vol
7,
197-223
Vaio
E
de,
Goni
B,

Rey
C
(1979)
Chromosomes
polymorphism
in
populations
of
the
grasshopper
Trimerotropis
pallidipennis
from
southern
Argentina.
Chromosoma,
71,
371-386
White
M
(1949)
A
cytological
survey
of
wild
populations
of
Trimerotropis
and

Circotettix.
I.
The
chromosomes
of
twelve
species.
Genetics
34,
537-563
White
M
(1951)
Cytogenetics
of
Orthopteroid
insects.
Adv
Genet
4,
267-330